4.1 Population genomics of Ceratitis capitata
The present study is the first using reduced-representation sequencing
genome in combination with a microbial characterisation in the medflyC. capitata , using samples from key geographic locations to
investigate the species’ population history and microbiome on a global
scale. We find strong evidence for two genetic clusters corresponding to
the South African individuals and the other localities in the introduced
range, in agreement with virtually all previous studies using allozymes
(Gasperi et al., 2002; Gasperi et al., 1991; Kourti, 2004; Malacrida et
al., 1992), mitochondrial DNA markers (Arias et al., 2018; Elfékih et
al., 2010; Elfékih, Makni, & Haymer, 2013; Karsten, van Vuuren,
Barnaud, & Terblanche, 2013; Ruiz-Arce et al., 2020), and
microsatellites (Bonizzoni et al., 2004; M. Bonizzoni et al., 2001;
Deschepper et al., 2021; Karsten et al., 2015; Nikolouli et al., 2020).
In addition, when we analysed the five sampling sites from the
introduced range separately (i.e., removing the South African samples),
populations from Brazil represented a unique genetic cluster that had
not been recognised in previous studies. The Brazil cluster was also
characterised by a distinct microbiome and the highest overall bacterial
diversity.
Karsten et al. (2013, 2015) observed high genetic diversity in South
African medflies due to a large number of alleles present at low
frequency, including many private alleles, which led them to suggest
that this population was ancestral and has maintained a large population
size over time. Other studies have shown that populations derived from
the African lineage exhibited a gradual decrease in genetic variation
(Malacrida et al., 2007; Deschepper et al., 2021 and references
therein), first to the Mediterranean basin populations and a second
towards American populations, thus dividing the colonisation process of
the medfly in three main categories: Ancestral populations (Sub-Sahara
and Africa), ancient populations (Mediterranean basin) and recent
populations (America) (Gasperi et al., 2002; Malacrida et al., 1998).
Our results showed a different pattern of genetic variation: across the
introduced range, most of the sampled locations belong to the same big
genetic cluster, indicating gene flow among these locations, except for
Brazil.
Gasperi et al. (2002), using allozymes, found similar levels
of genetic variability in South American populations (i.e., Argentina,
Brazil and Peru) to African ancestral populations, and they stated that
these populations did not have enough time to reach equilibrium and
further differentiation. Furthermore, Nikolouli et al. (2020) described
a discrete genetic cluster in some South American populations
(Argentina, Brazil and Bolivia) using microsatellites; however, they
stressed that this genetic cluster was not clearly distinct from other
medfly populations worldwide. Our study identified high genetic
diversity and a genetically distinct cluster of medflies collected in
Brazil. These findings suggest that some South American populations
might be derived from different genetic sources.
The combination of population structure and ABC analyses with
supervised machine learning allowed us to reconstruct the most probable
evolutionary scenario of C. capitata. It is important to note
that only a portion of the total geographical distribution of medfly is
covered in this study. Nevertheless, our limited data set was able to
support the initial divergence from South African ancient populations
that gave rise to populations in Brazil at a different time than those
in the rest of the world. These findings are partially congruent with
historical records of medfly distributions (Malacrida et al., 1998),
which medfly colonisation route may have occurred through the
transatlantic trade of enslaved people, as has been described
in D. melanogaster , which is also a descendant from the
Afrotropical region (David & Capy, 1988). Furthermore, the medfly
museum collections at the Natural History Museum of London provided
historical records to support this suggested new colonisation route. We
found that in the collection, the oldest record was dated in 1904, with
specimens collected in the tropical Saint Helena Island (Fig. 1). This
island, a UK overseas territory located in the South Atlantic Ocean,
midway between Africa and South America, was an important port during
the crown colony and an obligate stop for the Trans-Atlantic trade in
the colonial period. The human population in Saint Helena has genomic
traces linking them with Central-West African populations, moved during
the slavery years (Sandoval-Velasco et al., 2019). This colonisation
route for the medfly, different from the one connecting the
Mediterranean area and South America, had been mentioned by Gasperi et
al. (2002) and Ruiz-Arce et al. (2020) but has never been probed at the
genetic level. Our results modify the previous belief that only
Mediterranean basin medfly populations had contributed to the
colonisation of South America, as described in previous publications
(Deschepper et al., 2021; Malacrida et al., 1998; Malacrida et al.,
2007), and points out new potential ancestry sources for the genetic
units in the South American populations that need further
investigation.